Antioxidants
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antioxidants Article Puffing as a Novel Process to Enhance the Antioxidant and Anti-Inflammatory Properties of Curcuma longa L. (Turmeric) 1, 1, 2 1, 1, Yohan Choi y, Insu Ban y, Hyungjae Lee , Moo-Yeol Baik * and Wooki Kim * 1 Department of Food Science and Biotechnology, Graduate School of Biotechnology, Kyung Hee University, Yongin 17104, Korea; [email protected] (Y.C.); [email protected] (I.B.) 2 Department of Food Engineering, Dankook University, Cheonan 31116, Korea; [email protected] * Correspondence: [email protected] (M.-Y.B.); [email protected] (W.K.); Tel.: +82-31-201-2525 (M.-Y.B.); +82-31-201-3482 (W.K.) Authors equally contributed to the current work. y Received: 7 October 2019; Accepted: 23 October 2019; Published: 23 October 2019 Abstract: Curcuma longa L. (turmeric) is used as a food spice; however, its strong taste restricts wider applications as a food ingredient despite its well-known health benefits. To develop an effective yet simple process for enhancing its antioxidant and anti-inflammatory activities, turmeric was gun-puffed at various pressures. Puffed turmeric exhibited an increase in its brown color and porous structures, indicating the occurrence of the Maillard reaction and vaporization during the process. Proximal analysis revealed that puffing did not alter the major constituents, although a very small decrease in crude fat extraction was observed under some circumstances. Total phenolic compounds in the extract were significantly increased after puffing, and subsequent assessment of antioxidant capacity, as determined using independent 2,2-diphenyl-1-picrylhydrazyl (DPPH), 2,2’-azino-bis (3-ethylbenzothiazoline-6-sulphonic acid) (ABTS), and ferric reducing antioxidant power (FRAP) assays, demonstrated enhanced antioxidant capacity in a puffing-pressure-dependent manner. Turmeric extract was further tested for the regulation of inflammatory responses in the murine macrophage RAW264.7 cell line. Suppression of pro-inflammatory cytokines interleukin (IL)-6 and tumor necrosis factor (TNF)-α in lipopolysaccharides (LPS)-induced macrophages was amplified using puffed-turmeric extracts compared to the control extract. Furthermore, macrophage-activation assessment revealed downregulated expression of inflammation-relevant cluster of differentiation (CD)80 and CD86 using puffed-turmeric extract in a puffing-pressure-dependent manner. However, expression of major histocompatibility complex (MHC)-II, which controls adoptive immunity, was not affected by treatment with any of the turmeric extracts. Overall, the current study demonstrated that puffing is a promising and simple method for enhancing the antioxidant and anti-inflammatory properties of turmeric. Keywords: turmeric; curcuminoid; puffing; antioxidant; anti-inflammatory 1. Introduction Curcuma longa L. (turmeric) is a perennial herbaceous plant belonging to the genus Curcuma in the Zingiberaceae family and is cultivated throughout Asia. In addition to its use as a food spice, turmeric has long been used as a traditional medicine in India [1]. Recent studies have identified its major active compounds to include 4–6% curcuminoids, 2–4% essential oils, and 2–3% fixed oils [2]. Curcuminoids, the principal pigment and bioactive compounds in turmeric, are composed of curcumin (1,7-bis-(4-hydroxy-3-methoxyphenyl-1,6-heptadiene-3,5-dione) and its derivatives demethoxycurcumin (DMC) and bisdemethoxycurcumin (BDMC), which have been widely Antioxidants 2019, 8, 506; doi:10.3390/antiox8110506 www.mdpi.com/journal/antioxidants Antioxidants 2019, 8, 506 2 of 12 studied for antioxidant, anticancer, antimutagenic, and antibacterial functions [3–5]. The major component, curcumin, is a polyphenolic compound classified as generally recognized as safe (GRAS) by the U.S. Food and Drug Administration [6,7]. Despite its health benefits, turmeric, as well as its products, are limited in food applications due to its unique flavor and pungent taste. The low stability and bioavailability of curcuminoids also restrict the use of turmeric. Puffing, a cooking process using heat and pressure, is classified into two types: an atmospheric pressure method called oven puffing and a pressure drop method called gun puffing [8]. Both methods are based on vaporization of the moisture in the matrix of the food material; however, gun puffing induces expansion of the material through a sudden opening of a heated chamber to decrease the pressure [9]. Consequently, puffing contributes to physical changes in a solid including volume expansion, increased porosity, and decreased hardness. In addition, evaporation of water during the puffing process aids in the extension of the product’s shelf life. Chemical changes, including starch gelatinization and the Maillard reaction, noted in plant-derived foods also occur during puffing [10]. The Maillard reaction generates browning pigments and volatile substances, such as formic acid, acetaldehyde, formaldehyde, and glyoxal, which impart desirable flavors to the material [11]. In addition, puffing increases the antioxidant activity and extraction yield of bioactive compounds of doraji (Platycodon grandiflorum), cacao beans (Theobroma cacao L.), and ginseng (Panax ginseng C.A Meyer) [9,12,13]. Therefore, puffing is a potential treatment for various food materials, including turmeric, to improve functionality and palatability [14–16]. Inflammation is a complicated immune response to either exogenous irritators or internal damaged tissues. Therefore, inflammation itself is an essentially physiological component of the host defense, yet uncontrolled responses, termed chronic inflammation, are detrimental. Chronic inflammation can cause rheumatoid arthritis, psoriasis, multiple sclerosis, various cancers, and type I diabetes [17–19], and macrophages are key players in both the initiation and resolution of inflammation [20,21]. Therefore, many studies have attempted to regulate inflammatory responses in macrophages using various herbal extracts to prevent and/or ameliorate chronic inflammation. Although the anti-inflammatory effects of turmeric extract have been previously reported [22], the current study sought to determine the optimal conditions for puffing to maximize the functionality of turmeric extracts. In this regard, the extraction yield and health-aiding functions of extracts of turmeric with or without puffing were examined. 2. Materials and Methods 2.1. Materials and Chemicals Sliced and dried turmeric (cultivated in Jindo-gun, Republic of Korea, and harvested in October–December 2017) was purchased from Bibong Herb Co. (Yangju-si, Republic of Korea). Food-grade 70% ethanol was purchased from Ethanol Supplies World Co. (Jeonju-si, Republic of Korea), and methanol, sodium carbonate, sodium hydroxide, and hydrochloric acid were purchased from Daejung Chemicals & Metals Co. (Siheung-si, Republic of Korea). Folin–Ciocalteu’s phenol reagent, 2,20-azino-bis(3-ethylbenzothiazoline-6-sulfonic acid) diammonium salt (ABTS), 2,20-azobis(2-amidino-propane) dihydrochloride (AAPH), 1,1-diphenyl-2-picrylhydrazyl (DPPH), gallic acid, catechin, and ascorbic acid were purchased from Sigma Aldrich Co. (St. Louis, MO, USA). Aluminum chloride and sodium nitrite were purchased from Junsei Chemical Co., LTD (Tokyo, Japan). 2.2. Puffing Process The puffing of turmeric was carried out in the presence of four parts by weight dried rice to prevent excessive carbonization in the high temperatures while achieving the target pressure more quickly, as previously reported [15]. Briefly, a mixture of turmeric and rice was placed in the chamber of a rotary gun puffing machine and heated. Subsequently, the internal pressure of the chamber was increased to either 686, 784, 882, or 980 kPa, at which point the chamber door was suddenly opened to Antioxidants 2019, 8, 506 3 of 12 induce puffing through the rapid pressure release. Non-puffed turmeric served as a control, and all samples were stored at 20 C until the subsequent experiments − ◦ 2.3. Proximate Analysis The control or puffed turmeric samples were ground in a commercial blender (SFM-353NK, Shinil Industrial Co., Ltd., Cheonan-si, Korea) and sieved through a 20-mesh screen. The moisture, crude ash, crude fat, and crude protein contents were measured according to the Korean Food Standard Codex. Briefly, the moisture content was determined using oven drying at 105 ◦C and the crude fat content was measured using the Soxhlet extraction method. The crude protein content was calculated from the measured nitrogen content using the Kjeldahl method with 6.25 as the nitrogen–protein conversion factor. The ash content was determined from the weight of the turmeric following burning at 600 ◦C for 24 h. 2.4. Colorimetric Measurement The color difference in ground turmeric following puffing was measured using a colorimeter (JC801, Color Techno System, Tokyo, Japan). All measurements were performed on triplicate samples. The Hunter L-, a-, and b-value coordinates ranged from L = 0 (black) to 100 (white), a = 80 (green) to − 100 (red), and b = 80 (blue) to 70 (yellow). The values were calibrated with a white standard plate of − x = 93.82, y = 95.67, and z = 113.78. 2.5. Extraction A total of 200 mL of 70% ethanol was added to 5 g of ground turmeric (20:1, v/dried w), followed by stirring with a magnet at room temperature for 30 min. The extracts were vacuum filtered and the filtrate was stored at 20 C until subsequent experiments. To determine the extraction yield, − ◦ the extracts were dried at 105 ◦C in a drying oven (HB-502M, HanBaek Scientific Co., Bucheon-si, Korea), and the yield was calculated using: (w2 w ) E Extraction yield (%) = − 1 100 (1) A × E0 × where A is the weight of the turmeric (g), E is the total volume of the extract (mL), E’ is the used volume of extract (mL), w1 is the initial weight of the aluminum dish (g), and w2 is the weight of the aluminum dish and the solid (g). 2.6. Measurement of Total Phenolic and Total Flavonoid Contents The total polyphenol content (TPC) of turmeric was measured using Folin and Ciocalteu’s method [23]. Briefly, 200 µL of extract, 2.6 mL of distilled water, and 200 µL of Folin–Ciocalteu solution were reacted for 6 min. Following the reaction, 2 mL of Na2CO3 was added, and the absorbance was measured at 750 nm after 90 min.